OPEN
SUBJECT AREAS:
PALAEOECOLOGY
PALAEOCLIMATE
CLIMATE-CHANGE ECOLOGY
Increase in penguin populations during
the Little Ice Age in the Ross Sea,
Antarctica
Qi-Hou Hu1*, Li-Guang Sun1*, Zhou-Qing Xie1*, Steven D. Emslie2 & Xiao-Dong Liu1
BIOGEOCHEMISTRY
1
Received
21 June 2013
Accepted
5 August 2013
Published
22 August 2013
Correspondence and
requests for materials
should be addressed to
L.-G.S. (slg@ustc.edu.
cn) or Z.-Q.X. (zqxie@
ustc.edu.cn)
* These authors
contributed equally to
this work.
Institute of Polar Environment, School of Earth and Space Sciences, University of Science and Technology of China, Hefei 230026,
China, 2Department of Biology and Marine Biology, University of North Carolina Wilmington, 601 S. College Road, Wilmington,
NC 28403, USA.
Penguins are an important seabird species in Antarctica and are sensitive to climate and environmental
changes. Previous studies indicated that penguin populations increased when the climate became warmer
and decreased when it became colder in the maritime Antarctic. Here we determined organic markers in a
sediment profile collected at Cape Bird, Ross Island, high Antarctic, and reconstructed the history of Adélie
penguin colonies at this location over the past 700 years. The region transformed from a seal to a penguin
habitat when the Little Ice Age (LIA; 1500–1800 AD) began. Penguins then became the dominant species.
Penguin populations were the highest during ca. 1490 to 1670 AD, a cold period, which is contrary to
previous results in other regions much farther north. Different responses to climate change may occur at low
latitudes and high latitudes in the Antarctic, even if for same species.
P
enguin colonies are high-density breeding sites that also support plants such as algae, mosses and lichens1.
They thus form a simple and important terrestrial ecosystem in Antarctica. Using bioelements and organic
markers in the sediments from an accumulation of penguin guano, it has been possible to reconstruct
historical changes of penguin populations and plant communities, and their responses to environmental and
climatic changes at many sites around Antarctica1–8. Nevertheless, these studies were all conducted north of 70u S.
The Ross Sea region is a higher latitude embayment and contains a disproportionate number of Adélie penguins
(Pygoscelis adeliae), which occur only in the Antarctic, and considerable information exists on the occupation
history of this species in this region9–14. However, continuous records of penguin populations and associated plant
communities over the last millennium would provide a better understanding of the evolution of ecosystems under
changing climate15,16. Herein, we describe findings from a sediment profile (MB6) collected at an active Adélie
penguin colony along the northwest beach of Cape Bird, Ross Island in this region (166u269 44.40 E, 77u129 47.50 S;
Figure 1 and 2). This profile could represent at least a spatial range of 5 km (see Methods). By analyzing organic
molecular markers in the profile, we were able to reconstruct the penguin and vegetation records over the past 700
years to better understand the relationship between penguins and climate change in the high latitude Ross Sea
region.
Results
Sterols from droppings of animals can be used to indicate fecal contamination. In previous studies, cholesterol
and cholestanol were used as indicators for historical penguins, and phytol was used as the indicator for total
vegetation1,2. The sum of cholesterol and cholestanol is significantly correlated with traditional proxies such as
total organic carbon (TOC), total nitrogen (TN), and phosphorus (P)17 (Figure 3b–d), and was used as the
indicator for penguin populations in this study. Compared to traditional indices, these organic molecular markers
are better at distinguishing the influence between vegetative growth and animal activities. It is notable that the
TOC, N, and P concentrations increased prior to the increase of sterols and phytol. This result might be related to
the transformation of this location from a seal to a penguin habitat at ,1490 AD (see below). The two species
probably had different influences on the input of sterols TOC, N and P as well as plant growth. n-Alkanols with
even numbers of carbon atoms were also discovered in the sediments (Figure S1), with different arrays of carbon
atoms originating from different sources. Around the sampling site, algae and lichens currently are the main
species of vegetation. C18-ol and C28-ol were chosen as indicators for algae and lichens, respectively1,2. In addition,
n-alkanoic acids and n-Alkanes as well as pristane and phytane were simultaneously detected (Figures S2 and S3).
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Figure 1 | Maps of our sampling site on Cape Bird, Ross Island, as well as sampling sites of sediment cores Y23, Y46 and ZOL48 for penguins and ice
cores from Taylor Dome25 and Mt. Erebus Saddle19. These maps were created using CorelDRAW software.
Because they are not well correlated with penguin population
changes, we discuss them in the supplementary information.
Historical record of penguins, seals and vegetation in the past 700
years. The history of the Adélie penguin population and vegetation
abundance at Cape Bird during the past 700 years was reconstructed
using molecular markers (Figure 3). According to the variation of
these markers, the past 700 years were divided into four periods:
Period I: 1280–1490 AD; Period II: 1490–1670 AD; Period III:
1670–1950 AD; Period IV: 1950 AD–present.
Cholesterol and cholestanol were detected at the bottom of this
profile, indicating the sampling site had been contaminated by animal feces since ca. 1280 AD. The sum of cholesterol and cholestanol
increased slowly during this period. However, cholesterol and cholestanol cannot distinguish the influence of penguins from that of
other animals. In our previous study, seal hairs were observed below
32 cm of the sediment profile (corresponding to ca. 1490 AD), and
abruptly increased below 35 cm17. We interpret this finding as indicating that the sampling site was primarily a seal haulout and molting
location during Period I. Total vegetation abundance, as indicated by
phytols, remained at low levels throughout this period. From ca.
1490 AD onward, the concentrations of cholesterol 1 cholestanol
increased quickly, and total vegetation abundance displayed a similar
trend. Contrarily, seal hairs disappeared from the sediment, suggesting that seals moved from this locale and penguins then began to
occupy it. During Period II, penguin populations and total vegetation
abundance remained at high levels. The abundance of the two species
of plants also increased early in this period and algae stayed at a high
level, while lichens abruptly decreased and disappeared. At ca.
1670 AD, the penguin population and vegetation abundance
decreased and remained at low levels during Period III. Algae abundance decreased with the penguin population, but both temporarily
recovered at ca. 1850–1890 AD. Contrarily, lichens rapidly recovered with the decline of the penguin population and stayed at relatively high levels throughout this period. From ca. 1950 AD, penguin
populations continuously grew, which was supported by the observation in Cape Royds from 1959 to 199518.
Evolution of the penguin colonies: animals and plants. In
Antarctica, with its limited terrestrial biodiversity, penguin (or
seal) colonies and associated plants represent a simple ecosystem.
The droppings of penguins and seals contribute to the formation of
soil and provide nutrients for vegetation. Around these colonies,
algae, mosses and lichens grow in the enriched soils. Mosses did
not occur around our sampling site; algae were the dominant
plants compared to a limited number of lichens growing on the
surface of stones. According to previous studies, algae need a large
amount of nutrients input via penguin guano. Lichens need lower
nutrient input but are endangered by the trampling of penguins1,2.
Therefore, algae abundance is dependent on the presence of
penguins, while lichens have a contrary trend (Figure 3f–g). As the
total amount of vegetation is controlled by algae, the variation of the
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total vegetation abundance was similar to the trend of penguin (or
seal) populations in the past 700 years. The correlation coefficient
between cholesterol 1 cholestanol and phytol was calculated at 0.86
(R2 5 0.74).
Discussion
The Ross Sea region experienced the LIA from ca. 1500 to 1800 AD19,
when the summer temperature was about 2uC colder than that
during the past 200 years20. Organisms are apt to synthesize more
unsaturated fatty acids at low temperatures21,22. Kawamura and
Ishiwatari23 observed greater ratios of fatty acids C1852/C1850 during
colder periods in a sediment core collected in Lake Biwa, Japan, a
method also applied successfully in Antarctica24. For our samples, the
C1852/C1850 ratios showed little variation aside from a few samples.
However, during Period II which was optimum for penguins (shaded
areas in Figure 4), C1850 was absent at the depths of 22.2 (1660 AD),
25.8 (1620 AD), 28.2 (1570 AD), and 29.4 cm (1550 AD), indicating
cold conditions. Low temperatures during Period II are supported by
ice core record of stable isotopes (dD) at Taylor Dome (77u479470 S,
158u439260 E) where a trough during this period is evident25
(Figure 4g). Moreover, a core from the Mt. Erebus Saddle
(77u30.99 S, 167u40.599 E) also records a downtrend from ca.
1500 AD19 (Figure 4f). In general, the southern Ross Sea region
was abandoned by breeding Adélie penguins for 900 years until ca.
850 AD11, though a radiocarbon date on eggshell from one abandoned site at the south colony of Cape Bird indicates an earlier
appearance there, prior to our Period I at 690–960 AD (Emslie,
unpublished.). Further, our data support those of Polito, et al.10 in
that the north colony at Cape Bird was used only as a molting site by
penguins until about 1250 AD.
For the northwest beach of Cape Bird, the history of Adélie penguin colonies was even shorter, from ca. 1490 AD. Then the population rapidly increased and remained at markedly higher levels
Figure 2 | Photo of the sampling site taken by X. D. Liu.
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Figure 3 | Variation in penguin or seal populations with vegetation
abundance from proxy indices in the sediment profile MB6 at Cape bird
over the past 700 years. (a), population change; Cholesterol 1 cholestanol
concentrations represented seal population during Period I and
represented penguin population during Period II, III and IV. (b), (c) and
(d), traditional inorganic indexes (TOC, TN and P) for penguins; the
original data were reported by Nie, et al.17. (e), the change of total
vegetation abundance indicated by phytol concentrations. (f), algae
abundance change indicated by C18-ol concentrations. (g), lichen
abundance change indicated by C28-ol concentrations.
during this cold interval than during later periods. Nevertheless, this
trend is contrary to results from other regions much farther north. At
Zolotov Island, East Antarctica (68u399 S, 77u529 E), and Ardley
Island, Antarctic Peninsula (62u139 S, 58u569 W; Figure 1), Adélie
penguin populations stayed at relatively low levels during our Period
II3,6,8 (Figure 4b–d). Furthermore, previous studies at low latitudes in
the Antarctic have indicated that penguin populations, including
Adélie, Gentoo (Pygoscelis papua) and Chinstrap penguins
(Pygoscelis antarctica), increased when the climate became warmer
and decreased when it became colder1–8.
Penguin population dynamics are affected by variations of climatic and environmental factors, such as sea surface temperature,
air temperature, sea ice extent, snow cover, wind and the abundance
of food4,8,18,26,27. Both extremely high and low temperature is seemingly unfavorable for the survival of pygoscelid penguins28.
Temperature influences penguins mainly by driving change in these
environmental conditions. Increasing temperature may result in
increased snow-fall29. Thick snow cover prevents penguins from
building nests early enough in the summer to complete the nesting
cycle, thereby affecting the penguin population productivity and
growth29,30. During the LIA, the decreased snow accumulation in
the Ross Sea region20 likely favored breeding penguins. More importantly, sea surface temperature as well as prevailing winds indirectly
affect penguin populations by controlling sea ice extent and concentration31. During cold periods, increased sea ice can prevent beach
access by penguins to their colonies. Moreover, more northerly sea
ice extent may make it difficult for penguins to reach the food-rich
waters which are south of the southern boundary of the Antarctic
Circumpolar Current32. The lack of food affects the survival of penguins, especially juveniles and subadults. In this manner climate
affects the trends in penguin populations over 100 s to 1000 s of
years. In the Ross Sea, Adélie penguin colonies have appeared and
disappeared throughout this region over the past 8000 years in response to these environmental variables11. A warm period at 4000–
2000 BP, the penguin ‘optimum’14, saw an expansion in penguin
colonies in the southern Ross Sea. The optimum in this study
(Period IV) is a warm period with a reduction in sea ice extent18 that
also favors penguin population expansion.
However, the influence of sea ice is critical. Algae under sea ice is
an important food source for krill33, which in turn is an important
prey for penguins. Thus, extended sea ice provides abundant krill and
subsequently has a remarkable impact on the supply of food for
penguins. Besides the increased sea ice extent, prevailing katabatic
winds also increased in the Ross Sea during the LIA20. Strong winds
caused sea-ice to split and created more polynya areas in the Ross
Sea19. Larger size of polynya favors beach access by penguins to their
colonies and increases the proportion of breeding penguins34.
Furthermore, prevalent katabatic winds during the LIA were adverse
to snow precipitation and resulted in decreased snow accumulation20, which favored the breeding of penguins.
Beside climatic and environmental changes, emigrations also
cause local variations in penguin populations. Penguins began to
occur at our sampling site when seals abandoned it at ca. 1490 AD,
the beginning of the LIA. Obviously, these penguins emigrated
from other locations. This emigration might be associated with
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Figure 4 | Proxy indices of penguin populations and climate records. The shaded areas correspond to Period II, an optimum for penguins.
(a), penguin population changes from the sediment profile MB6 at Cape Bird as indicated by the sums of cholesterol and cholestanol concentrations.
(b), penguin population changes from the sediment core ZOL48 at Zolotov Island as indicated by the P concentrations. (c) and (d), penguin population
changes from the sediment cores Y23 and Y46 at Ardley Island as indicated by the P concentrations. (e), climate changes from the dD records in the
Mt. Erebus Saddle ice core (100-points smoothed); the original data were reported by Rhodes, et al.19. (f), climate changes from the dD records in the
Taylor Dome ice core (3-points smoothed); the original data were reported by Steig, et al.25.
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showed a record of about 120 years. 14C ages were determined by accelerator mass
spectrometry(AMS)using the guano sediments as well as hairs and bones in the
sediments. The 14C ages were calibrated for the marine carbon reservoir effect using a
DR 5 750 6 50 yr11 and the CALIB 4.3 software program with the INTCAL98
calibration dataset39. Combined with seven 210Pb dates and four 14C dates, a
polynomial curve5 was fitted to the age-depth relationship (Figure 5). The profile
represents about 700 years of deposition.
Figure 5 | Chronology of the sediment profile MB6. The ages were
determined by 210Pb dates and 14C dates, and the age-depth relationship
was fitted with a cubic polynomial.
deteriorating environmental conditions in southern regions when
the LIA began. The movement of penguins and thus alterative population distributions has been documented in the Ross Sea region35
and Terra Nova Bay region (74u539 S, 163u459 E)36. This emigration
of penguins to the sampling site may be accomplished in a short time
and causes abruptly elevated populations. For instance, the movement of Adélie penguins to new breeding sites could occur over 1–2
decades in the Windmill Islands, East Antarctica37. This study suggests possibly different response to climate change by penguins at low
latitudes and high latitudes in the Antarctic. The increased polynya
accompanied by more convenient access to open water, abundant
food for penguins, decreased snow-fall, as well as emigration from
other sites might have been drivers for the increase in penguin populations during the LIA. Nonetheless, the MB6 sediment profile could
record historical penguins in limited spatial range. More continuous
records of penguins are needed for a better understanding of the
population dynamics at high latitudes in the Antarctic.
Methods
Sampling. The sediment profile and core series MBs (McMurdo Sound and Cape
Bird) were collected during an investigation in the Ross Sea region in January, 201017.
The sediment profile for this study (MB6) was obtained from a catchment on the
second terrace above sea level at Cape Bird on the north side of Ross Island (Figure 1
and 2). The MB6 profile was collected from a pit excavated at the sampling site.
Breeding penguins spread from the sampling site to higher terraces at about 300 m
above the sea level, covering an extent of more than 5 km. The MB6 profile recorded
the historical penguin populations in this spatial range. Seals were not discovered
around the sampling site. The profile was directly sectioned in the field at 0.6 cm
intervals and then stored in a freezer at 220uC until analysis. The detailed procedures
for sampling are described elsewhere17.
Chemical analysis. Thirty-two samples of the sectioned sediment profile were
selected for organic analysis. Before analysis, sediment samples were freeze-dried and
ground through a 140 mesh screen. Details of the analytical procedure for molecular
markers was previously described1,2. Briefly, the dried sediment samples were Soxhlet
extracted for 72 h with 180 mL mixed solvent (dichloromethane:methanol 251, V/
V). The extracts were concentrated by rotary evaporation and afterwards saponified
using 0.5 M KOH dissolved in methanol. Then each of the saponified extracts was
divided into three portions (hydrocarbons fraction, alcohols fraction and acids
fraction) through controlling chemical conditions. Neutral lipids were partitioned out
of each saponified extract with hexane. Acidic lipids were separated by adjusting PH
to 2 with 0.5 M HCl and then extracted with mixed solvent (dichloromethane:hexane
159, V/V). Neutral lipids were further divided on 5% deactivated silica gel column
chromatography using different solvents of increasing polarity. Hydrocarbons were
eluted with hexane and then alcohols, including n-alkanols and sterols, were eluted
with ethyl acetate. The alcohols and acids fractions were silylanized with N,O-bis(trimethylsilyl)-trifluoroacetamide (BSTFA) to form trimethylsilyl (TMS)-ether
derivatives, and then analyzed by a gas chromatography–mass selective detector.
Dating. The chronology of the sediment profile MB6 was determined by 14C dating
and 210Pb dating. The detailed method was described elsewhere5,38. The top 4.2 cm
sediments were analyzed for 210Pb with Ortec HPGe GWL series detectors and
SCIENTIFIC REPORTS | 3 : 2472 | DOI: 10.1038/srep02472
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Acknowledgements
This research was supported by grants from the National Natural Science Foundation of
China (Project Nos. 40231002, 41025020), the Chinese Arctic and Antarctic
Administration (Projects Nos. CHINARE2013-04-01, CHINARE2013-04-04), the
Fundamental Research Funds for the Central Universities. Field work at Cape Bird was
supported by a National Science Foundation grant (ANT 0739575) to S. Emslie with
logistical support from Raytheon Polar Services. We thank David G. Ainley for his helpful
comments on this manuscript. The authors acknowledge the State Key Laboratory of
Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Science
(CAS) for all analysis performed there.
Author contributions
Q.H.H., Z.Q.X. and L.G.S. contributed equally to the design of the study and preparation of
the manuscript. S.D.E. contributed to the discussion of results and manuscript refinement.
X.D.L. and S.D.E. contributed to the sample collection. Q.H.H., Z.Q.X. and L.G.S.
contributed to analysis.
Additional information
Supplementary information accompanies this paper at http://www.nature.com/
scientificreports
Competing financial interests: The authors declare no competing financial interests.
How to cite this article: Hu, Q.-H., Sun, L.-G., Xie, Z.-Q., Emslie, S.D. & Liu, X.-D. Increase
in penguin populations during the Little Ice Age in the Ross Sea, Antarctica. Sci. Rep. 3,
2472; DOI:10.1038/srep02472 (2013).
This work is licensed under a Creative Commons AttributionNonCommercial-NoDerivs 3.0 Unported license. To view a copy of this license,
visit http://creativecommons.org/licenses/by-nc-nd/3.0
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